Current models of bacterial genome evolution suggest that in small populations a burst of transposable element activity may lead to inactivation of non-essential genes and large deletions, followed by erosion of the pseudogenes resulting in genome reduction. Due to this process, the smallest sequenced cellular genomes are all obligate intracellular symbionts of insects. Interestingly, it seems that the presence of symbionts in small populations within each host reduces the efficacy of the purifying selection increasing the genetic drift that increase the fixation of deleterious mutations.
The evolutionary scenarios seem to be quite different for eukaryotic symbionts since they have different evolutionary patterns of their genomes and it has been reported the gain of mobile genetic elements and intronic sequences resulting in larger genomes.
A recent paper by Kevin J. Vogel and Nancy A. Moran compared the evolution of symbiont analyzing a monophyletic group of aphids within the subfamily Cerataphidinae that have lost the bacterial symbiont common to all other Aphididae (Buchnera aphidicola), which have been replaced by a eukaryotic one, the Yeast-Like Symbiont (YLS). In particular, Vogel and Moran used this system as a model to test the hypothesis that chronically high levels of genetic drift will result in an increase in size of a eukaryotic symbiont genome.
Sequencing of the Yeast-Like Symbiont genome revealed, unlike the obligate bacterial symbionts that lost several genes for DNA repair and recombination, the YLS appears to have fully functional recombinational machinery, including the full suite of genes necessary for meiotic division. Furthermore, the YLS’s genome reveals a diverse suite of metabolic abilities unlike the streamlined metabolism of the obligate bacterial symbionts of insects, though it has lost many genes found in related fungi. At this regards, like Buchnera, the YLS encodes the full biosynthesis pathways for essential amino acids, though it can also produce the non-essential amino acids, which Buchnera mostly receives from the host. The ability of the YLS to produce essential amino acids supports the hypothesis that the YLS has replaced Buchnera’s functional role in these aphids.
The genome of the YLS resulted enriched in introns and presented an elevated rates of amino acid substitution but no burst in mobile DNAs has been observed so that the YLS genome do not support the hypothesis of rampant genome expansion observed in fungi such as Tuber melanosporum. The high gene density and small intergenic spacers suggest that YLS may reside in a range of population size and genome size that allow for expansion of introns but limit the rampant proliferation of mobile genetic elements.
As a whole, the patterns observed in the YLS genome suggest that its symbiotic lifestyle is permissive to intron proliferation and accelerated sequence evolution, though other factors appear to limit its overall genome expansion. This result could suggest the intron and mobile DNA gains occur in different times, but the Buchnera-aphid symbiosis is much older, and is thought to originate at least 200 mya so that the relatively young association of YLS with hosts may not have permitted sufficient time to allow for genome expansion.
Vogel KJ, & Moran NA (2013). Functional and evolutionary analysis of the genome of an obligate fungal symbiont. Genome biology and evolution PMID: 23563967